Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish

Abstract

Little is known regarding the coordination of audition with decision-making and subsequent motor responses that initiate social behavior including mate localization during courtship. Using the midshipman fish model, we tested the hypothesis that the time spent by females attending and responding to the advertisement call is correlated with the activation of a specific subset of catecholaminergic (CA) and social decision-making network (SDM) nuclei underlying auditory- driven sexual motivation. In addition, we quantified the relationship of neural activation between CA and SDM nuclei in all responders with the goal of providing a map of functional connectivity of the circuitry underlying a motivated state responsive to acoustic cues during mate localization. In order to make a baseline qualitative comparison of this functional brain map to unmotivated females, we made a similar correlative comparison of brain activation in females who were unresponsive to the advertisement call playback. Our results support an important role for dopaminergic neurons in the periventricular posterior tuberculum and ventral thalamus, putative A11 and A13 tetrapod homologues, respectively, as well as the posterior parvocellular preoptic area and dorsomedial telencephalon, (laterobasal amygdala homologue) in auditory attention and appetitive sexual behavior in fishes. These findings may also offer insights into the function of these highly conserved nuclei in the context of auditory-driven reproductive social behavior across vertebrates.

Sound‐induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally‐breeding songbird

“…20,30 In the present study, we tested whether sound-induced increases in monoaminergic activity are higher in response to song than to a control sound, and whether they depend on endocrine state ( Figure 1A, Question 1). On the basis of popular models, in which monoamines modulate auditory responses in accordance with the behavioural relevance of the stimulus, 2,27,[53][54][55][56] we predicted that hearing song, but not a behaviourally irrelevant tone sequence, would increase monoaminergic turnover in the auditory pathway.…”

Brain Activation Patterns in Response to Conspecific and Heterospecific Social Acoustic Signals in Female Plainfin Midshipman Fish, <b><i>Porichthys notatus</i></b>

“…After 30 minutes of continuous exposure to one of the three acoustic stimuli, the subjects were removed from the testing cage and were then kept individually in a 5 gallon bucket filled with water from the intertidal for an additional 120 minutes before being sacrificed. The 120 minute post-treatment time before sacrifice was chosen to allow adequate cFos synthesis after sound exposure based on the work by Petersen et al (2013) and Forlano et al (2017). Fish were first deeply anesthetized in a 0.025% aminobenzoate bath after which they were weighed and measured for standard length (SL) before being transcardially perfused with ice cold teleost ringers followed by 4% paraformaldehyde in 0.1 M Phosphate buffer (PB; pH 7.2).…”

“…Post-hoc Tukey tests were used to make pair-wise comparisons across groups for each nucleus. Correlations between water temperature and cFos-ir activity were conducted and the Benjamini-Hochberg procedure was used to correct for multiple comparisons with a false discovery rate of 0.25 (Butler and Maruska 2016, Forlano et al 2017). All statistics were analyzed using IBM SPSS Statistics 19 and GraphPad Prism 5 software.…”

Ecology of fish hearing

“…Furthermore, one of the most widely studied group of sonic fishes, the Batrachoididae (toadfishes and midshipmen), produce low frequency boatwhistles (40–250 Hz; Maruska & Mensinger, ) and hums (90–140 Hz; Ibara et al ., ) to attract females to their nest (Fine & Lenhardt, ). Females exhibit auditory driven sexual motivation by responding to the advertisement calls of males (Forlano et al ., ). The calling rate and calling effort (percentage of time spent calling) of Lusitanian toadfish Halobatrachus didactylus (Bloch & Schneider 1801) has also been found to indicate male condition (Vasconcelos et al ., ) because these variables reflect sonic muscle hypertrophy and larger gonads (Amorim et al ., ).…”